Through the eyes of a mouse lemur – understanding the evolutionary emergence of visual cortical columns through cellular imaging, optimization theory, and visual behavior in a miniature primate

Fred Wolf - MPI for Dynamics and Self-Organization, Georg-August-Universität Göttingen
Daniel Huber - Université de Genève

Functional cortical columns, groups of neurons of similar tuning properties vertically spanning the layers of the cerebral cortex, are widely considered a fundamental unit of neocortical organization. In the primary visual cortex (V1) of primates and carnivores key examples are orientation columns, local groups of neurons responding to visual contours of similar orientation. Recent research on rodent visual cortex, however, has established beyond reasonable doubt that such an arrangement of orientation selective neurons in functional cortical columns is not universal but one of at least two possible design alternatives: In rodents such as mice, rats, and squirrels V1 neurons of different orientation preferences are spatially intermingled in a distinct “salt-and-pepper” pattern. Accumulating evidence suggests that not only the cells’ positioning but also the neuronal circuits of the visual cortical network are distinctly different between rodents and primates. Nevertheless, rodents and primates are closely related, with rodents likely retaining the organization of the visual cortex of their common ancestor. Thus, after their divergence, brain evolution in the primate lineage must have led to a fundamental transformation of visual cortical circuitry. The nature and adaptive value of this transformation, however, are not well understood. Paleobiological studies have reconstructed the first true primates as small nocturnal, arboreal foragers and hunters of the tropical forest. Studies of vision and visual cortex in species that share or retain these traits, lifestyle, and habitat thus promise to elucidate the nature of the fundamental transformation in visual cortical circuits leading to the emergence of functional cortical columns. Do intermediate visual cortical circuit architectures exist? If yes, what are their features? And which evolutionary forces and mechanisms might have driven the fundamental reorganization of visual cortex near the origin of modern primates? Here we address these questions in theoretical and experimental studies of visual cortex and visually guided behavior of the mouse lemur (Microcebus murinus), a basal strepsirhine primate.